Hostname: page-component-76fb5796d-9pm4c Total loading time: 0 Render date: 2024-04-28T16:03:04.955Z Has data issue: false hasContentIssue false
  • English
  • Français

Capsicum frutescens and Citrus limon: a new take on therapy against experimental trichinellosis

Published online by Cambridge University Press:  25 May 2021

Marwa Ahmed Mohamed Salama ,
Nahed E. Mostafa ,
Naglaa Fathy Abd El-Aal ,
Eman M. Mostafa ,
Samar Kamel Hammad ,
Rasha Adel  and
Howayda Said Fouad Moawad Open the ORCID record for Howayda Said Fouad Moawad [Opens in a new window]
Marwa Ahmed Mohamed Salama
Affiliation:
Department of Medical parasitology, Faculty of medicine, Zagazig University, Zagazig44159, Egypt
Nahed E. Mostafa
Affiliation:
Department of Medical parasitology, Faculty of medicine, Zagazig University, Zagazig44159, Egypt
Naglaa Fathy Abd El-Aal
Affiliation:
Department of Medical parasitology, Faculty of medicine, Zagazig University, Zagazig44159, Egypt
Eman M. Mostafa
Affiliation:
Department of Medical parasitology, Faculty of medicine, Zagazig University, Zagazig44159, Egypt
Samar Kamel Hammad
Affiliation:
Department of Medical parasitology, Faculty of medicine, Zagazig University, Zagazig44159, Egypt
Rasha Adel
Affiliation:
Department of Pharmacognosy, Faculty of Pharmacy, Zagazig University, Zagazig44159, Egypt
Howayda Said Fouad Moawad*
Affiliation:
Department of Medical parasitology, Faculty of medicine, Zagazig University, Zagazig44159, Egypt
*
Author for correspondence:Howayda Said Fouad Moawad, E-mail: drhowaydasaid@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Trichinellosis is a zoonotic disease that endangers human health and can lead to death. Restricted absorption and poor results of conventional therapies demand new effective natural remedies to treat both enteral and parenteral trichinellosis. This study assessed the antiparasitic and anti-inflammatory effects of Citrus limon and Capsicum frutescens on murine trichinellosis and compared them with those of albendazole and prednisolone, which are conventionally used to treat trichinellosis. Overall, 50 Swiss albino male mice were divided into five groups, with ten mice in each group: negative control, positive control, albendazole combined with prednisolone, C. limon, and C. frutescens. Mice were sacrificed 7 and 35 days after infection, for intestinal and muscular phase analyses. Drug efficacies were parasitologically, biochemically, histopathologically and ultrastructurally assessed. Our results demonstrated the efficacy of C. frutescens and C. limon extracts as antiparasitic agents, showing a substantial decrease in adult and larval counts. Moreover, both extracts had the ability to decrease serum tumour necrosis factor-α levels during the intestinal and muscular phases. In addition to the improved histopathological changes in the small intestine and muscles, the destructive effects on adults and larvae were ultrastructurally evident on transmission electron microscopy. In conclusion, C. frutescens and C. limon extracts are promising remedies for the treatment of experimental trichinellosis, particularly, the C. frutescens extract.

Keywords

murine trichinellosiscitrus limoncapsicum frutescensplant extractstransmission electron microscopyTNF-α
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e26
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

AL-Attar, TA, El-Kersh, WM, Sadek, GS, Harba, NM, Osheiba, SF and Brakat, RM (2020) A study of immunotherapeutic efficacy of Trichinella spiralis excretory-secretory proteins in murine trichinellosis. Journal of Egyptian Society of Parasitology 50, 281–292.CrossRefGoogle Scholar
Alvarado, R., Meza, L., García, M., Saldívar, S. & Moreno, G. (1996) Hormonal effect on the parasite load in the infection by T. spiralis of a murine experimental model. Trichinellosis. In 9th International Conference on Trichinellosis (ICT9). In Ortega P, Wakelin eds.Google Scholar
Anthony, OE, Ese, AC and Lawrence, EO (2013) Regulated effects of Capsicum frutescens supplemented diet (CFSD) on fasting blood glucose level, biochemical parameters and body weight in alloxan induced diabetic Wistar rats. British Journal of Pharmaceutical Research 3, 496.CrossRefGoogle Scholar
Attia, RA, Mahmoud, AE, Farrag, HMM, Makboul, R, Mohamed, ME and Ibraheim, Z (2015) Effect of myrrh and thyme on Trichinella spiralis enteral and parenteral phases with inducible nitric oxide expression in mice. Memórias do Instituto Oswaldo Cruz 110, 1035–1041.CrossRefGoogle ScholarPubMed
Basyoni, MM and El-Sabaa, AA (2013) Therapeutic potential of myrrh and ivermectin against experimental Trichinella spiralis infection in mice. Korean Journal of Parasitology 51(3), 297–304.CrossRefGoogle ScholarPubMed
Bauri, RK, Tigga, MN and Kullu, SS (2015) A review on use of medicinal plants to control parasites. Indian Journal of Natural Products and Resources 6, 268–277.Google Scholar
Bruschi, F (2012) Trichinellosis in developing countries: Is it neglected? Journal of Infection in Developing Countries 6, 216–222.CrossRefGoogle ScholarPubMed
Bruschi, F. and Dupouy-Camet, J. (2014) Trichinellosis. Helminth Infections and their Impact on Global Public Health Bruschi, F. (Ed.). Vienna, Springer Vienna, 229-273.CrossRefGoogle Scholar
Caner, A, Döşkaya, M, Değirmenci, A, Can, H, Baykan, Ş, Üner, A, Başdemir, G, Zeybek, U and Gürüz, Y (2008) Comparison of the effects of Artemisia vulgaris and Artemisia absinthium growing in western Anatolia against trichinellosis (Trichinella spiralis) in rats. Experimental Parasitology 119, 173–179.CrossRefGoogle ScholarPubMed
Chen, TT, Peng, S, Wang, Y, Hu, Y, Shen, Y, Xu, Y, Yin, J, Liu, C and Cao, J (2019) Improvement of mitochondrial activity and fibrosis by resveratrol treatment in mice with Schistosoma japonicum infection. Biomolecules 9(11), 658.CrossRefGoogle ScholarPubMed
Elgendy, D, Othman, AA, Hasby, SM, et al. (2020) Resveratrol reduces oxidative damage and inflammation in mice infected with Trichinella spiralis. Journal of Helminthology 94(e140), 1–10.CrossRefGoogle ScholarPubMed
Gilleard, J and Beech, RN (2007) Population genetics of anthelmintic resistance in parasitic nematodes. Parasitology 134, 1133–1147.CrossRefGoogle ScholarPubMed
Gomes, MS, Cardoso, MdG, Soares, MJ, Batista, LR, Machado, SM, Andrade, MA, de Azeredo, CM, Resende, JMV and Rodrigues, L (2014) Use of essential oils of the genus Citrus as biocidal agents. American Journal of Plant Sciences 5, 299–305.CrossRefGoogle Scholar
Karunovsky, M (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. Journal of Cell Biology 27, 137A.Google Scholar
Kaur, K, Jain, M, Kaur, T and Jain, R (2009) Antimalarials from nature. Bioorganic & Medicinal Chemistry 17, 3229–3256.CrossRefGoogle ScholarPubMed
Kawaguchi, K, Kikuchi, S, Hasegawa, H, Maruyama, H, Morita, H and Kumazawa, Y (1999) Suppression of lipopolysaccharide-induced tumor necrosis factor-release and liver injury in mice by naringin. European Journal of Pharmacology 368, 245–250.CrossRefGoogle ScholarPubMed
Kiernan, J.A. (1999) Histological and histochemical methods: Theory and practice, 3rd Edition. Shock 12:479.CrossRefGoogle Scholar
Kisiel, K and Kaszuba, A (2011) Alclometasone dipropionate: Properties and clinical uses. Postepy Dermatologii i Alergologii 28, 120.Google Scholar
Klimek-Szczykutowicz, M, Szopa, A and Ekiert, H (2020) Citrus limon (lemon) phenomenon-A review of the chemistry, pharmacological properties, applications in the modern pharmaceutical, food, and cosmetics industries, and biotechnological studies. Plants (Basel, Switzerland) 9, 119.Google ScholarPubMed
Kurian, J. (2007) Plants that heals, 1st edn, Pune. Oriental Watchman Publishing House,2, 53.Google Scholar
Lee, TH, Lee, JG, Yon, JM, Oh, KW, Baek, IJ, Nahm, SS, Lee, BJ, Yun, YW and Nam, SY (2011) Capsaicin prevents kainic acid-induced epileptogenesis in mice. Neurochemistry International 58, 634–640.CrossRefGoogle ScholarPubMed
Loos, JA, Dávila, VA, Rodrígues, CR, Petrigh, R, Zoppi, JA, Crocenzi, FA and Cumino, AC (2017) Metformin exhibits preventive and therapeutic efficacy against experimental cystic echinococcosis. PLoS Negl Trop Dis 9,11(2), e0005370.Google ScholarPubMed
Luft, JH (1961) Improvements in epoxy resin embedding methods. The Journal of Cell Biology 9, 409–414.CrossRefGoogle ScholarPubMed
Madhumathy, AP, Aivazi, A and Vijayan, VA (2007) Larvicidal efficacy of Capsicum annum against Anopheles stephensi and Culex quinquefasciatus. The Journal of Vector Borne Diseases 44, 223–226.Google ScholarPubMed
Manzur, AY, Kuntzer, T, Pike, M and Swan, A (2008) Glucocorticoid corticosteroids for Duchenne muscular dystrophy. Cochrane Database Systematic Review 23(1), CD003725.Google Scholar
Mayer-Scholl, A, Pozio, E, Gayda, J, Thaben, N, Bahn, P and Nöckler, K (2017) Magnetic stirrer method for the detection of Trichinella larvae in muscle samples. J. Vis. Exp 121, e55354.Google Scholar
Muñoz-Carrillo, JL, Muñoz-Escobedo, JJ, Maldonado-Tapia, C, Chávez-Ruvalcaba, F and Moreno-García, MA (2017) Resiniferatoxin lowers TNF-α, NO and PGE2 in the intestinal phase and the parasite burden in the muscular phase of Trichinella spiralis infection. Parasite Immunology 39, e12393.CrossRefGoogle ScholarPubMed
Muñoz-Carrillo, JL, Maldonado-Tapia, C, López-Luna, A, Muñoz-Escobedo, JJ, Flores-De La Torre, JA and Moreno-García, A (2018) Current aspects in Trichinellosis. In Selection of our books indexed in the Book. Citation Index In Web of Science TM Core Collection (BKCI) Parasites and Parasitic Diseases. doi: 10.5772/intechopen.80372.Google Scholar
Nascimento, P, Nascimento, T, Ramos, N, Silva, G, Câmara, C, Silva, T, Moreira, K and Porto, A (2013) Antimicrobial and antioxidant activities of Pimenta malagueta (Capsicum frutescens). African Journal of Microbiology Research 7, 3526–3533.Google Scholar
Neves, WdS, Freitas, LGd, Coutinho, MM, Dallemole-Giaretta, R, Fabry, CdFS, Dhingra, OD and Ferraz, S (2009) Nematicidal activity of extracts of red hot chili pepper, mustard and garlic on Meloidogyne javanica in green house. Summa Phytopathologica 35, 255–261.CrossRefGoogle Scholar
Otunola, GA, Afolayan, AJ, Ajayi, EO and Odeyemi, SW (2017) Characterization, antibacterial and antioxidant properties of silver nanoparticles synthesized from aqueous extracts of Allium sativum, Zingiber officinale, and Capsicum frutescens. Pharmacognosy Magazine 13, S201–S208.CrossRefGoogle ScholarPubMed
Park, MK, Kang, YJ, Jo, JO, Baek, KW, Yu, HS, Choi, YH, Cha, HJ and Ock, MS (2018) Effect of muscle strength by Trichinella spiralis infection during chronic phase. International Journal of Medical Sciences 15, 802–807.CrossRefGoogle ScholarPubMed
Piekarska, JSM, Michalski, A, Obminska-Mrukowicz, B and Gorczykowski, M (2010) The effect of immunomodulating drugs on the percentage of apoptotic and necrotic lymphocytes in inflammatory infiltrations in the muscle tissue of mice infected with Trichinella spiralis. Polish Journal of Veterinary Sciences 13, 233–240.Google ScholarPubMed
Prichard, RK (2007) Markers for benzimidazole resistance in human parasitic nematodes? Parasitology 134, 1087–1092.CrossRefGoogle ScholarPubMed
Rayia, DMA, Saad, AE, Ashour, DS and Oreiby, RM (2017) Implication of artemisinin nematocidal activity on experimental trichinellosis: In vitro and in vivo studies. Parasitology International 66, 56–63.CrossRefGoogle ScholarPubMed
Ren, Y, Qin, Y, Zhang, X, Zheng, L, Dai, X and Wu, H (2018) Killing the muscular larvae of Trichinella spiralis and the anti-fibrotic effect of the combination of Wortmannilatone F and recombinant G31P in a murine model. Biomedicine & Pharmacotherapy 108, 934–940.CrossRefGoogle ScholarPubMed
Rosskopf Erin, N, Therrien Leonard, L, Adkins Scott, T, Iriarte, F, Foster Joyce, G and Kokalis-Burelle, N (2008) Methods of reducing pests and treating gastrointestinal nematode infections. U.S. Patent Application No. 12/006,523, filed July 10, 2008.Google Scholar
Schneider, CA, Rasband, WS and Eliceiri, KW (2012) NIH image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.CrossRefGoogle ScholarPubMed
Shalaby, M, Moghazy, F, Shalaby, H and Nasr, S (2010) Effect of methanolic extract of Balanites aegyptiaca fruits on enteral and parenteral stages of Trichinella spiralis in rats. Parasitology Research 107, 17–25.CrossRefGoogle ScholarPubMed
Shang, K, Amna, T, Amina, M, Al-Musayeib, NM, Al-Deyab, SS and Hwang, I (2017) Influence of capsaicin on inflammatory cytokines induced by lipopolysaccharide in myoblast cells under in vitro environment. Pharmacognosy Magazine 13, S26–S32.Google ScholarPubMed
Shoheib, ZS, Shamloula, MM, Abdin, AA and El-Segai, O (2006) Role of α-chymotrypsin and colchicine as adjuvant therapy in experimental muscular trichinellosis: Parasitological, biochemical and immunohistochemical study. Egyptian Journal of Medical Microbiology 15, 773–790.Google Scholar
Squires, JM, Foster, JG, Lindsay, DS, Caudell, DL and Zajac, AM (2010) Efficacy of an orange oil emulsion as an anthelmintic against Haemonchus contortus in gerbils (Meriones unguiculatus) and in sheep. Veterinary Parasitology 172, 95–99.CrossRefGoogle Scholar
Sukontason, KL, Chaiwong, T, Chaisri, U, Kurahashi, H, Sanford, M and Sukontason, K (2011) Reproductive organ of blow fly, Chrysomya megacephala (Diptera: Calliphoridae): Ultrastructural of testis. Journal of Parasitology Research 2011, 690863. doi: 10.1155/2011/690863.CrossRefGoogle ScholarPubMed
Suvarna, SK, Layton, C and Bancroft, JD (2013) Bancroft's theory and practice of histological techniques. 7th Edition. Philadelphia, Churchill Livingstone of Elsevier.Google Scholar
Tag, HM, Kelany, OE, Tantawy, HM and Fahmy, AA (2014) Potential anti-inflammatory effect of lemon and hot pepper extracts on adjuvant-induced arthritis in mice. The Journal of Basic & Applied Zoology 67, 149–157.CrossRefGoogle Scholar
Upadhyaya, S (2018) Citrus limon L burmf peel: Potential anthelmintic agent against Indian earthworm Eicinia foetida. Journal of Drug Delivery and Therapeutics 8, 248–250.CrossRefGoogle Scholar
Vasconcelos, VO, Martins, MAD, de Oliveira, NJ and Duarte, ER (2014) Effect of ethanolic extract of Capsicum frutescens L. on adult female of Rhipicephalus microplus (Ixodidae). Parasitology Research 113(4), 1389–1394.CrossRefGoogle Scholar
Vinayaka, KS, Nandini, KC, Rakshitha, MN, Ramya, M, Shruthi, J, Shruthi, V, Prashith, KTR and Raghavendra, HL (2010) Proximate composition, antibacterial and anthelmintic activity of Capsicum frutescens (L.) Var. Longa (Solanaceae) leaves. Pharmacognosy Journal 2, 486–491.CrossRefGoogle Scholar
Yadav, AK and Temjenmongla, (2012) Efficacy of Lasia spinosa leaf extract in treating mice infected with Trichinella spiralis. Parasitology Research 110, 493–498.CrossRefGoogle ScholarPubMed
Youmsi, R, Tsouh Fokou, PV, Menkem, E, Bakarnga-Via, I, Keumoe, R, Nana, V and Boyom, F (2017) Ethnobotanical survey of medicinal plants used as insects repellents in six malaria endemic localities of Cameroon. Journal of Ethnobiology and Ethnomedicine 13, 33. doi: 10.1186/s13002-017-0155-x.CrossRefGoogle ScholarPubMed
Yu, L, Yan, J and Sun, Z (2017) D-limonene exhibits anti-inflammatory and antioxidant properties in an ulcerative colitis rat model via regulation of iNOS, COX-2, PGE2 and ERK signaling pathways. Molecular Medicine Reports 15(4), 2339–2346.CrossRefGoogle Scholar
Zeng, Z, Wang, Q, Yang, X, et al. (2019) Qishen granule attenuates cardiac fibrosis by regulating TGF-β /Smad3 and GSK-3β pathway. Phytomedicine 62, 152949.CrossRefGoogle ScholarPubMed
Zhang, QW, Lin, LG and Ye, WC (2018) Techniques for extraction and isolation of natural products: A comprehensive review. Chinese Medicine 13(1), 20.CrossRefGoogle ScholarPubMed
Zimmer, AR, Leonardi, B, Zimmer, ER, Kalinine, E, Onofre de Souza, D, Portela, LV and Gosmann, G (2012) Long-term oral administration of Capsicum baccatum extracts does not alter behavioral, hematological, and metabolic parameters in CF1 mice. Evidence-Based Complementary and Alternative Medicine 2012, 196358. doi:10.1155/2012/196358.CrossRefGoogle Scholar